Abstract
This study aims to investigate the effects of individuals’ exposure to rare earth elements (REEs) on bone metabolism. Adopting the inductively coupled plasma mass spectrometry, we measured REEs and eight other elements (Ca, Fe, Cu, Na, K, Zn, Mg, and P) in the hair of 53 miners exposed to REEs from Baiyunebo and 57 healthy farmers as the control group. Furthermore, bone mineral density (BMD) in both groups was assessed by dual-energy X-ray absorptiometry. Analysis of variance showed that the concentrations of La, Ce, Pr, Nd, Tb, Ho, Tm, and Yb in male hair of exposed group were significantly higher compared with the control group, whereas the concentrations of Ca and Fe in exposed group were significantly lower; the results of female hair, except for Ce, Tb, Ho, Tm, and Yb, were consistent with male hair. Student’s t test showed that the BMD of exposed males at lumbar vertebrae, femoral neck, greater trochanter, and intertrochanter was significantly lower than that of controls, and exposed females reported lower BMD values at lumbar vertebrae and femoral neck. Multiple linear regression analysis showed that concentrations of differential REEs were inversely related to BMD in males, and concentrations of Ca and Fe were positively related to BMD both in males and females. Our study suggests that long-term environmental and occupational exposure leads to REE accumulation, and a low level of iron and calcium due to the competitive binding of REEs, which together induce bone metabolism disorders, and further reduce BMD.
Similar content being viewed by others
References
Wang L, Liang T (2016) Anomalous abundance and redistribution patterns of rare earth elements in soils of a mining area in Inner Mongolia, China. Environ Sci Pollut Res 23(11):11330–11338. https://doi.org/10.1007/s11356-016-6351-8
Liu C, Hou Y, Gao M (2014) Are rare-earth nanoparticles suitable for in vivo applications? Adv Mater 26(40):6922–6932. https://doi.org/10.1002/adma.201305535
Pagano G, Aliberti F, Guida M, Oral R, Siciliano A, Trifuoggi M, Tommasi F (2015) Rare earth elements in human and animal health: state of art and research priorities. Environ Res 142(11):215–220. https://doi.org/10.1016/j.envres.2015.06.039
Gwenzi W, Mangori L, Danha C, Chaukura N, Dunjana N, Sanganyado E (2018) Sources, behaviour, and environmental and human health risks of high-technology rare earth elements as emerging contaminants. Sci Total Environ 636(9):299–313. https://doi.org/10.1016/j.scitotenv.2018.04.235
Wang B, Yan L, Huo W, Lu Q, Cheng Z, Zhang J, Li Z (2017) Rare earth elements and hypertension risk among housewives: a pilot study in Shanxi Province, China. Environ Pollut 220(Pt B):837–842. https://doi.org/10.1016/j.envpol.2016.10.066
Ze Y, Cheng J, Cai J, Cheng Z, Hu R, Hong F (2011) The impairment of liver DNA conformation and liver apoptosis of mice caused by CeCl3. Biol Trace Elem Res 143(1):437–445. https://doi.org/10.1007/s12011-010-8880-1
Zhao H, Hong J, Yu X, Zhao X, Sheng L, Ze Y, Sang X, Gui S, Sun Q, Wang L, Hong F (2013) Oxidative stress in the kidney injury of mice following exposure to lanthanides trichloride. Chemosphere 93(6):875–884. https://doi.org/10.1016/j.chemosphere.2013.05.034
Wu J, Yang J, Lu X, Jin C, Wu S, Zhang L, Hu X, Ma H, Cai Y (2019) Lanthanum chloride impairs the blood-brain barrier integrity by reduction of Junctional proteins and upregulation of MMP-9 in rats. Biol Trace Elem Res 187(2):482–491. https://doi.org/10.1007/s12011-018-1402-2
Panyala A, Chinde S, Kumari SI, Grover P (2017) Assessment of genotoxicity and biodistribution of nano- and micron-sized yttrium oxide in rats after acute oral treatment. J Appl Toxicol 37(12):1379–1395. https://doi.org/10.1002/jat.3505
Zhao H, Cheng Z, Hu R, Chen J, Hong M, Zhou M, Gong X, Wang L, Hong F (2011) Oxidative injury in the brain of mice caused by lanthanid. Biol Trace Elem Res 142(2):174–189. https://doi.org/10.1007/s12011-010-8759-1
Grimaldi A, Mocumbi AO, Freers J, Lachaud M, Mirabel M, Ferreira B, Narayanan K, Celermajer DS, Sidi D, Jouven X, Marijon E (2016) Tropical endomyocardial fibrosis: natural history, challenges, and perspectives. Circulation 133(24):2503–2515. https://doi.org/10.1161/circulationaha.115.021178
Semelka RC, Prybylski JP, Ramalho M (2019) Influence of excess ligand on nephrogenic systemic fibrosis associated with nonionic, linear gadolinium-based contrast agents. Magn Reson Imaging 58(5):174–178. https://doi.org/10.1016/j.mri.2018.11.015
Schieda N, Blaichman JI, Costa AF, Glikstein R, Hurrell C, James M, Jabehdar Maralani P, Shabana W, Tang A, Tsampalieros A, van der Pol C, Hiremath S (2018) Gadolinium-based contrast agents in kidney disease: comprehensive review and clinical practice guideline issued by the Canadian Association of Radiologists. Can Assoc Radiol J 69(2):136–150. https://doi.org/10.1016/j.carj.2017.11.002
Calabrese EJ, Baldwin LA (2003) Hormesis: the dose-response revolution. Annu Rev Pharmacol Toxicol 43:175–197. https://doi.org/10.1146/annurev.pharmtox.43.100901.140223
Liu D, Zhang J, Wang G, Liu X, Wang S, Yang M (2012) The dual-effects of LaCl(3) on the proliferation, osteogenic differentiation, and mineralization of MC3T3-E1 cells. Biol Trace Elem Res 150(1–3):433–440. https://doi.org/10.1007/s12011-012-9486-6
Zhang S, Liu Q, Li L, Bai Y, Yang B (2018) The controllable lanthanum ion release from Ca-P coating fabricated by laser cladding and its effect on osteoclast precursors. Mater Sci Eng C 93(12):1027–1035. https://doi.org/10.1016/j.msec.2018.08.059
You M, Li K, Xie Y, Huang L, Zheng X (2017) The effects of cerium valence states at cerium oxide coatings on the responses of bone mesenchymal stem cells and macrophages. Biol Trace Elem Res 179(2):259–270. https://doi.org/10.1007/s12011-017-0968-4
Huang J, Zhang TL, Xu SJ, Li RC, Wang K, Zhang J, Xie YN (2006) Effects of lanthanum on composition, crystal size, and lattice structure of femur bone mineral of Wistar rats. Calcif Tissue Int 78(4):241–247. https://doi.org/10.1007/s00223-005-0294-2
Hu Y, Du Y, Jiang H, Jiang GS (2014) Cerium promotes bone marrow stromal cells migration and osteogenic differentiation via Smad1/5/8 signaling pathway. Int J Clin Exp Pathol 7(8):5369–5378
Bai J, Wang XH, Zhang CJ, Huang J, Muller WEG (2018) Lanthanum-containing bioparticles are associated with the influence of lanthanum on high phosphate mediated bone marrow stromal cells viability. Biometals 31(5):771–784. https://doi.org/10.1007/s10534-018-0121-7
Kadir M, Wang X, Zhu B, Liu J, Harland D, Popescu C (2017) The structure of the “amorphous” matrix of keratins. J Struct Biol 198(2):116–123. https://doi.org/10.1016/j.jsb.2017.04.001
Pozebon D, Scheffler GL, Dressler VL (2017) Elemental hair analysis: a review of procedures and applications. Anal Chim Acta 992(11):1–23. https://doi.org/10.1016/j.aca.2017.09.017
Mikulewicz M, Chojnacka K, Gedrange T, Gorecki H (2013) Reference values of elements in human hair: a systematic review. Environ Toxicol Pharmacol 36(3):1077–1086. https://doi.org/10.1016/j.etap.2013.09.012
Zhuang M, Zhao J, Li S, Liu D, Wang K, Xiao P, Yu L, Jiang Y, Song J, Zhou J, Wang L, Chu Z (2017) Concentrations and health risk assessment of rare earth elements in vegetables from mining area in Shandong, China. Chemosphere 168:578–582. https://doi.org/10.1016/j.chemosphere.2016.11.023
Liu WS, Guo MN, Liu C, Yuan M, Chen XT, Huot H, Zhao CM, Tang YT, Morel JL, Qiu RL (2019) Water, sediment and agricultural soil contamination from an ion-adsorption rare earth mining area. Chemosphere 216:75–83. https://doi.org/10.1016/j.chemosphere.2018.10.109
Li X, Chen Z, Chen Z, Zhang Y (2013) A human health risk assessment of rare earth elements in soil and vegetables from a mining area in Fujian Province, Southeast China. Chemosphere 93(6):1240–1246. https://doi.org/10.1016/j.chemosphere.2013.06.085
Wei B, Li Y, Li H, Yu J, Ye B, Liang T (2013) Rare earth elements in human hair from a mining area of China. Ecotoxicol Environ Saf 96:118–123. https://doi.org/10.1016/j.ecoenv.2013.05.031
Hao Z, Li Y, Li H, Wei B, Liao X, Liang T, Yu J (2015) Levels of rare earth elements, heavy metals and uranium in a population living in Baiyun Obo, Inner Mongolia, China: a pilot study. Chemosphere 128:161–170. https://doi.org/10.1016/j.chemosphere.2015.01.057
Liu H, Wang J, Yang Z, Wang K (2015) Serum proteomic analysis based on iTRAQ in miners exposed to soil containing rare earth elements. Biol Trace Elem Res 167(2):200–208. https://doi.org/10.1007/s12011-015-0312-9
Tong SL, Zhu WZ, Gao ZH, Meng YX, Peng RL, Lu GC (2004) Distribution characteristics of rare earth elements in children’s scalp hair from a rare earths mining area in southern China. J Environ Sci Health Part A 39(9):2517–2532. https://doi.org/10.1081/ESE-200026332
Liang Q, Yin H, Li J, Zhang L, Hou R, Wang S (2018) Investigation of rare earth elements in urine and drinking water of children in mining area. Medicine (Baltimore) 97(40):e12717. https://doi.org/10.1097/MD.0000000000012717
Peng RL, Pan XC, Lu GC, Wang NF (2002) Distribution pattern of rare earth elements in hair samples of young children aged 0-3 yrs in rare earth ore area. J Environ Health 19(01):39–41
Zhu W, Xu S, Shao P, Zhang H, Wu D, Yang W, Feng J, Feng L (2005) Investigation on liver function among population in high background of rare earth area in South China. Biol Trace Elem Res 104(1):1–7. https://doi.org/10.1385/BTER:104:1:001
Chen XA, Cheng YE, Rong Z (2005) Recent results from a study of thorium lung burdens and health effects among miners in China. J Radiol Prot 25(4):451–460. https://doi.org/10.1088/0952-4746/25/4/007
Smith MP, Campbell LS, Kynicky J (2015) A review of the genesis of the world class Bayan Obo Fe–REE–Nb deposits, Inner Mongolia, China: multistage processes and outstanding questions. Ore Geol Rev 64(1):459–476. https://doi.org/10.1016/j.oregeorev.2014.03.007
Wu C (2008) Bayan Obo controversy: carbonatites versus iron oxide-Cu-Au-(REE-U). Resour Geol 58(4):348–354. https://doi.org/10.1111/j.1751-3928.2008.00069.x
Yuan Z, Bai G, Wu C, Zhang Z, Ye X (1992) Geological features and genesis of the Bayan Obo REE ore deposit, Inner Mongolia, China. Appl Geochem 7(5):429–442. https://doi.org/10.1016/0883-2927(92)90004-M
Drew LJ, Meng Q, Sun W (1990) The Bayan Obo iron-rare-earth-niobium deposits, Inner Mongolia, China. Lithos 26(1):43–65. https://doi.org/10.1016/0024-4937(90)90040-8
Pena-Fernandez A, Gonzalez-Munoz MJ, Lobo-Bedmar MC (2016) Evaluating the effect of age and area of residence in the metal and metalloid contents in human hair and urban topsoils. Environ Sci Pollut Res 23(21):21299–21312. https://doi.org/10.1007/s11356-016-7352-3
Drobyshev EJ, Solovyev ND, Ivanenko NB, Kombarova MY, Ganeev AA (2017) Trace element biomonitoring in hair of school children from a polluted area by sector field inductively coupled plasma mass spectrometry. J Trace Elem Med Biol 39(1):14–20. https://doi.org/10.1016/j.jtemb.2016.07.004
Watts NB (2004) Fundamentals and pitfalls of bone densitometry using dual-energy X-ray absorptiometry (DXA). Osteoporos Int 15(11):847–854. https://doi.org/10.1007/s00198-004-1681-7
Baker HM, Baker CJ, Smith CA, Baker EN (2000) Metal substitution in transferrins: specific binding of cerium(IV) revealed by the crystal structure of cerium-substituted human lactoferrin. J Biol Inorg Chem 5(6):692–698. https://doi.org/10.1007/s007750000157
Wang M, Lai TP, Wang L, Zhang H, Yang N, Sadler PJ, Sun H (2015) “Anion clamp” allows flexible protein to impose coordination geometry on metal ions. Chem Commun 51(37):7867–7870. https://doi.org/10.1039/c4cc09642h
Sasmaz A, Ozkan S, Gursu MF, Sasmaz M (2017) The hematological and biochemical changes in rats exposed to britholite mineral. Appl Radiat Isot 129(11):185–188. https://doi.org/10.1016/j.apradiso.2017.07.060
Feng L, He X, Xiao H, Li Z, Li F, Liu N, Chai Z, Zhao Y, Zhang Z (2007) Ytterbium and trace element distribution in brain and organic tissues of offspring rats after prenatal and postnatal exposure to ytterbium. Biol Trace Elem Res 117(1–3):89–104. https://doi.org/10.1007/BF02698086
Zhang H, Feng J, Zhu W, Liu C, Xu S, Shao P, Wu D, Yang W, Gu J (2000) Chronic toxicity of rare-earth elements on human beings: implications of blood biochemical indices in REE-high regions, South Jiangxi. Biol Trace Elem Res 73(1):1–17. https://doi.org/10.1385/BTER:73:1:1
Skalny AV, Skalnaya MG, Tinkov AA, Serebryansky EP, Demidov VA, Lobanova YN, Grabeklis AR, Berezkina ES, Gryazeva IV, Skalny AA, Skalnaya OA, Zhivaev NG, Nikonorov AA (2015) Hair concentration of essential trace elements in adult non-exposed Russian population. Environ Monit Assess 187(11):677. https://doi.org/10.1007/s10661-015-4903-x
Huang J, Xu SJ, Lu JF, Wang K (2001) Effect of rare earth ions in formation of calcium carbonate. J Chin Rare Earth Soc 19(05):478–480
Zhang J, Huang J, Xv S, Yu S, Zhang T, Yang M (2005) Effects of lanthanum on bone resorbing activity of rabbit mature osteoclasts co-cultured with osteoblasts. J Rare Earths 15(4):496–501
Zhang J, Zhang T, Xv S, Wang K, Yu S, Yang M (2005) Effect of lanthanum(III) on cytosolic free calcium in isolated rabbit mature osteoclasts. J Rare Earths 15(5):580–583
Liu D, Zhang J, Li Y, Wang S, Yang M (2012) The effects of Ce on the proliferation, osteogenic differentiation and mineralization function of MC3T3-E1 cells in vitro. Biol Trace Elem Res 149(2):291–297. https://doi.org/10.1007/s12011-012-9423-8
Li R, Yang H, Wang K (2003) La accumulation and microstructure change of leg bones of rats fed with La(NO3)3 in low dosage for a long term. Beijing Da Xue Xue Bao 35(6):622–624
Jiang C, Shang J, Li Z, Qin A, Ouyang Z, Qu X, Li H, Tian B, Wang W, Wu C, Wang J, Dai M (2016) Lanthanum chloride attenuates osteoclast formation and function via the downregulation of rankl-induced Nf-κb and Nfatc1 activities. J Cell Physiol 231(1):142–151. https://doi.org/10.1002/jcp.25065
Welldon KJ, Findlay DM, Evdokiou A, Ormsby RT, Atkins GJ (2013) Calcium induces pro-anabolic effects on human primary osteoblasts associated with acquisition of mature osteocyte markers. Mol Cell Endocrinol 376(1–2):85–92. https://doi.org/10.1016/j.mce.2013.06.013
Xiang B, Liu Y, Xie L, Zhao Q, Zhang L, Gan X, Yu H (2016) The osteoclasts attach to the bone surface where the extracellular calcium concentration decreases. Cell Biochem Biophys 74(4):553–558. https://doi.org/10.1007/s12013-016-0757-2
Messer JG, Cooney PT, Kipp DE (2010) Iron chelator deferoxamine alters iron-regulatory genes and proteins and suppresses osteoblast phenotype in fetal rat calvaria cells. Bone 46(5):1408–1415. https://doi.org/10.1016/j.bone.2010.01.376
Katsumata S, Tsuboi R, Uehara M, Suzuki K (2006) Dietary iron deficiency decreases serum osteocalcin concentration and bone mineral density in rats. Biosci Biotechnol Biochem 70(10):2547–2550. https://doi.org/10.1271/bbb.60221
Gorres KL, Raines RT (2010) Prolyl 4-hydroxylase. Crit Rev Biochem Mol Biol 45(2):106–124. https://doi.org/10.3109/10409231003627991
Jones G, Prosser DE, Kaufmann M (2014) Cytochrome P450-mediated metabolism of vitamin D. J Lipid Res 55(1):13–31. https://doi.org/10.1194/jlr.R031534
Acknowledgments
The authors wish to thank the study participants and Baiyunebo mining area for their contributions to this study.
Contributions
Liu HM: design and implementation of the study, research, and writing of the manuscript. Liu HY: design and implementation of the study, data analysis. Yang ZH and Wang KZ: supervision and review of the manuscript. All of the authors have read the manuscript and have agreed to submit it, in its current form, for consideration for publication.
Funding
The study was supported by Inner Mongolia Natural Science Foundation (No. 2018MS08146) and Baotou Medical College Science Foundation (No. BYJJ-YF 201730).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of Interest
The authors declare that they have no conflict of interest.
Ethical Approval
All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research ethics committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards. The study was approved by the Bioethics Committee of Baotou Medical College (No. BY17-86).
Consent to Participate
Informed consent was obtained from all individual participants included in the study.
Consent to Publish
Not applicable.
Additional information
Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Liu, H., Liu, H., Yang, Z. et al. Bone Mineral Density in Population Long-Term Exposed to Rare Earth Elements from a Mining Area of China. Biol Trace Elem Res 199, 453–464 (2021). https://doi.org/10.1007/s12011-020-02165-0
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12011-020-02165-0